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November 24, 2017

Soft selection for gentleness in Puerto Rican African Honeybees

Filed under: Population genetics,Population genomics,Soft Selection,Soft Sweep — Razib Khan @ 3:07 pm


When I was a kid “killer bees” were a major pop culture thing. There were movies about the bees, and we would get updates about their march northward in the news. They were a cautionary tale of our species’ hubris.

Today we have a little bit more perspective. These bees were actually just African honeybees, the ancestral population to European honeybees, which were introduced to the New World with Europeans centuries earlier than the African honeybees. African honeybees were not that different from European honeybees, but they were more aggressive and tended to outcompete European honeybee colonies. They are a major problem for the beekeeping industry, but not a major threat to human life.

Today the African and European populations in the United States seem to have stabilized in their ranges, with a hybrid zone between them. African bee’s migratory behavior makes them less competitive with European bees in colder climates.

A friend of mine once mentioned to me that if he had to do it all over again he would do research on the evolutionary genomics of Hymenoptera, and in particular bees. People care about bees. So it ‘s no surprise that I noticed this paper out in Nature Communications, A soft selective sweep during rapid evolution of gentle behavior in an Africanized honeybee:

Highly aggressive Africanized honeybees (AHB) invaded Puerto Rico (PR) in 1994, displacing gentle European honeybees (EHB) in many locations. Gentle AHB (gAHB), unknown anywhere else in the world, subsequently evolved on the island within a few generations. Here we sequence whole genomes from gAHB and EHB populations, as well as a North American AHB population, a likely source of the founder AHB on PR. We show that gAHB retains high levels of genetic diversity after evolution of gentle behaviour, despite selection on standing variation. We observe multiple genomic loci with significant signatures of selection. Rapid evolution during colonization of novel habitats can generate major changes to characteristics such as morphological or colouration traits, usually controlled by one or more major genetic loci. Here we describe a soft selective sweep, acting at multiple loci across the genome, that occurred during, and may have mediated, the rapid evolution of a behavioural trait.

Come for the bees, but stay for the soft selection! If you talk to anyone in evolutionary and population genomics you know that the future is in understanding patterns of soft selection and polygenic selection from standing variation. Though these are related phenomena which are associated with each other, all are all distinct.

Standing variation just refers to the diversity which is segregating in the population at any given time. At any given moment many loci exhibit polymorphism. This polymorphism can be a target of natural selection if it is correlated with heritable variation and differentials in fitness. Though soft selection can be quite wooly it’s inverse, hard selection, is clear: in genetic terms hard selection can be seen in allele frequency changes at a single variant in a locus, going from the point where it is a novel mutation to nearly fixed in the population. In Haldane’s original conception hard selection involved excess deaths, and imposed a limit on the rate of evolution as well as the amount variation you could expect within a given population. This model was convenient in the pre-genomic and early genomic era because empirical selection tests had to focus on large allele frequency changes around singular loci. Researchers didn’t have large numbers of whole-genome samples available (nor the computational ability to analyze them).

Today this is not a limitation. In the analysis above the authors had 30 individuals of the 3 populations sequenced at high quality (20x). They ended up with millions of genetic variants they could analyze.

The plot to the left shows that “gentle African honeybees” (gAHB) tend to be closer to the African honeybee populations (AHB) overall (though with some hybridization with European honeybees, EHB). This is not surprising.

But the key observation was that over 12 generations the African honeybees of Puerto Rico became progressively less aggressive, despite maintaining overall morphological similarities to the mainland Mexican African bees from which they likely derive. Though buried in the discussion, there is a rationale for why this morphological change may have occurred: the Puerto Rican bees are subject to a lot of negative selection against aggression because of the density of the island, as well as the reality that aside from humans there aren’t other many species where their aggressive tendencies are beneficial. Basically, if you are an aggressive colony, it’s harder to make a go in densely settled areas (the implication here then is that there are probably “gentle” African honeybee populations across Latin America, they just are never disaggregated from the broader meta-population).

Credit: Phillip Messer and Nandita Garud

It’s the genomics where the real evolutionary insight comes in: they found that there were multiple soft sweep events around genetic regions implicated in behavior. In their overall genome the gAHB of Puerto Rico resembled mainland AHB, but in this subset of genetic loci they resembled EHB. Many of these loci had also been known to be targets of selection when the original European bee population diverged from the ancestral African population. Basically this is a genomic illustration of convergent evolution.

Regular readers of this blog will recognize the ways they detected selection. They used a modified form of EHH, which is reasonable since the selection event was recent enough to have been associated with distinct haplotype blocks. Also, standard Fst analysis showed that these were outliers in relation to the broader genetic pattern of relatedness (these loci were more like EHB than AHB, while most loci were more like AHB than EHB).

So this a form of polygenic selection. Remember, natural selection only knows genes through the phenotype (with intra-genomic selection being an exception). A behavior like aggression is probably subject to the fourth law of behavior genetics. That is, variation won’t be defined around a single genetic locus. Rather, variation across the genome will be correlated with variation in the phenotype. As selection favors a particular value of the phenotype across the distribution the allele frequencies across many genetic loci will shift, but they will not necessarily fix. Polygenic selection operates on the dispersed standing genetic variation which explains much of the variation of the phenotype in question. Instead of total sweeps to fixation due to large fitness differences between a given allele and its alternative form, the selection impact is distributed and diffused across the genome.

Though most of the genetic variants seem to recapitulate the evolution of the less aggressive phenotype that occurred with the original migration north of African honeybees, some of the selection signatures were novel. This points to the reality that when you have soft selection on standing variation you may have similar phenotypes which evolve via different means. Additionally, the authors noted that these results were in contrast to controlled breeding experiments in mammals where selection for gentility (“domestication”) often targeted a few loci and exhibited strong pleiotropic effects (due to the genetic correlation). These results point to the limitations of inferences made from human-directed selection.

Soft selection is probably ubiquitous. Consider the evolution of skin color in humans. There are lots of variants and lots of variation, and most of the variation seems to be ancestral. Only at the locus SLC24A5 do you have a perfect illustration of a hard selective sweep, probably from a de novo mutation that emerged around the Last Glacial Maximum.

From a geneticists’ perspective evolution is basically conceived of as changes in allele frequencies over time. Much of this is due to natural selection. Now that the world of soft selection is opening up, I suspect that we’ll understand a lot more of what we see around us, at least in the generality.

Citation: A soft selective sweep during rapid evolution of gentle behaviour in an Africanized honeybee.

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